The role of DNA topoisomerase 1α (AtTOP1α) in regulating arabidopsis meiotic recombination and chromosome segregation

Author:

Elesawi Ibrahim Eid12ORCID,Hashem Ahmed M.13,Yao Li1,Maher Mohamed2,Hassanin Abdallah A.4ORCID,Abd El-Moneim Diaa5ORCID,Safhi Fatmah A.6,Al Aboud Nora M.7,Alshamrani Salha Mesfer8,Shehata Wael F.910,Chunli Chen111

Affiliation:

1. College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China

2. Agricultural Biochemistry Department, Faculty of Agriculture, Zagazig University, Zagazig, Egypt

3. Biotechnology Department, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt

4. Genetics Department, Faculty of Agriculture, Zagazig University, Zagazig, Egypt

5. Department of Plant Production, (Genetic Branch), Faculty of Environmental and Agricultural Sciences, Arish University, El-Arish, El-Arish, Egypt

6. Department of Biology, College of Science, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia

7. Department of Biology Faculty of Science, Umm Al‐Qura University, Makkah, Saudi Arabia

8. Department of Biological Science, College of Science, University of Jeddah, Jeddah, Saudi Arabia

9. College of Agriculture and Food Sciences, Department of Agricultural Biotechnology, King Faisal University, Al-Ahsa, Al-Ahsa, Saudi Arabia

10. College of Environmental Agricultural Science, Plant Production Department, Arish University, Arish, North Sinai, Egypt

11. National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, Huazhong Agricultural University, Wuhan, Hubei, China

Abstract

Meiosis is a critical process in sexual reproduction, and errors during this cell division can significantly impact fertility. Successful meiosis relies on the coordinated action of numerous genes involved in DNA replication, strand breaks, and subsequent rejoining. DNA topoisomerase enzymes play a vital role by regulating DNA topology, alleviating tension during replication and transcription. To elucidate the specific function of DNA topoisomerase 1α ($AtTOP1 \alpha$) in male reproductive development of Arabidopsis thaliana, we investigated meiotic cell division in Arabidopsis flower buds. Combining cytological and biochemical techniques, we aimed to reveal the novel contribution of $AtTOP1 \alpha$ to meiosis. Our results demonstrate that the absence of $AtTOP1 \alpha$ leads to aberrant chromatin behavior during meiotic division. Specifically, the top1α1 mutant displayed altered heterochromatin distribution and clustered centromere signals at early meiotic stages. Additionally, this mutant exhibited disruptions in the distribution of 45s rDNA signals and a reduced frequency of chiasma formation during metaphase I, a crucial stage for genetic exchange. Furthermore, the atm-2×top1α1 double mutant displayed even more severe meiotic defects, including incomplete synapsis, DNA fragmentation, and the presence of polyads. These observations collectively suggest that $AtTOP1 \alpha$ plays a critical role in ensuring accurate meiotic progression, promoting homologous chromosome crossover formation, and potentially functioning in a shared DNA repair pathway with ATAXIA TELANGIECTASIA MUTATED (ATM) in Arabidopsis microspore mother cells.

Funder

National Natural Science Foundation of China

Advanced Foreign Experts Project

Hubei Hongshan Laboratory

Princess Nourah bint Abdulrahman University

King Faisal University, Saudi Arabia

Publisher

PeerJ

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